Different forms of traumatic brain injuries cause different tactile hypersensitivity profiles

Anne-Sophie Wattiez; William C Castonguay; Olivia J Gaul; Jayme S Waite; Chantel M Schmidt; Alyssa S Reis; Brandon J Rea; Levi P Sowers; Coral J Cintrón-Pérez; Edwin Vázquez-Rosa; Andrew A Pieper; Andrew F Russo

doi:10.1097/j.pain.0000000000002103

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Different forms of traumatic brain injuries cause different tactile hypersensitivity profiles

Journal article

Peer reviewed

Different forms of traumatic brain injuries cause different tactile hypersensitivity profiles

Anne-Sophie Wattiez, William C Castonguay, Olivia J Gaul, Jayme S Waite, Chantel M Schmidt, Alyssa S Reis, Brandon J Rea, Levi P Sowers, Coral J Cintrón-Pérez, Edwin Vázquez-Rosa, …

Pain (Amsterdam), Vol.162(4), pp.1163-1175

04/01/2021

DOI: 10.1097/j.pain.0000000000002103

PMCID: PMC8008742

PMID: 33027220

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https://www.ncbi.nlm.nih.gov/pmc/articles/8008742View

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Abstract

Chronic complications of traumatic brain injury represent one of the greatest financial burdens and sources of suffering in the society today. A substantial number of these patients suffer from posttraumatic headache (PTH), which is typically associated with tactile allodynia. Unfortunately, this phenomenon has been understudied, in large part because of the lack of well-characterized laboratory animal models. We have addressed this gap in the field by characterizing the tactile sensory profile of 2 nonpenetrating models of PTH. We show that multimodal traumatic brain injury, administered by a jet-flow overpressure chamber that delivers a severe compressive impulse accompanied by a variable shock front and acceleration-deceleration insult, produces long-term tactile hypersensitivity and widespread sensitization. These are phenotypes reminiscent of PTH in patients, in both cephalic and extracephalic regions. By contrast, closed head injury induces only transient cephalic tactile hypersensitivity, with no extracephalic consequences. Both models show a more severe phenotype with repetitive daily injury for 3 days, compared with either 1 or 3 successive injuries in a single day, providing new insight into patterns of injury that may place patients at a greater risk of developing PTH. After recovery from transient cephalic tactile hypersensitivity, mice subjected to closed head injury demonstrate persistent hypersensitivity to established migraine triggers, including calcitonin gene-related peptide and sodium nitroprusside, a nitric oxide donor. Our results offer the field new tools for studying PTH and preclinical support for a pathophysiologic role of calcitonin gene-related peptide in this condition.

Details

Title: Subtitle: Different forms of traumatic brain injuries cause different tactile hypersensitivity profiles
Creators: Anne-Sophie Wattiez - Center for the Prevention and Treatment of Visual Loss, Veterans Administration Health Center, Iowa City, IA, United States
William C Castonguay - Center for the Prevention and Treatment of Visual Loss, Veterans Administration Health Center, Iowa City, IA, United States
Olivia J Gaul - Department of Molecular Physiology and Biophysics, University of Iowa, Iowa City, IA, United States
Jayme S Waite - Department of Molecular Physiology and Biophysics, University of Iowa, Iowa City, IA, United States
Chantel M Schmidt - Department of Molecular Physiology and Biophysics, University of Iowa, Iowa City, IA, United States
Alyssa S Reis - Department of Molecular Physiology and Biophysics, University of Iowa, Iowa City, IA, United States
Brandon J Rea - Center for the Prevention and Treatment of Visual Loss, Veterans Administration Health Center, Iowa City, IA, United States
Levi P Sowers - Center for the Prevention and Treatment of Visual Loss, Veterans Administration Health Center, Iowa City, IA, United States
Coral J Cintrón-Pérez - Institute for Transformative Molecular Medicine, School of Medicine, Case Western Reserve University, Cleveland, OH, United States
Edwin Vázquez-Rosa - Institute for Transformative Molecular Medicine, School of Medicine, Case Western Reserve University, Cleveland, OH, United States
Andrew A Pieper - Department of Neuroscience, Case Western Reserve University, School of Medicine, Cleveland, OH, United States
Andrew F Russo - Department of Neurology, University of Iowa, Iowa City, IA, United States
Resource Type: Journal article
Publication Details: Pain (Amsterdam), Vol.162(4), pp.1163-1175
DOI: 10.1097/j.pain.0000000000002103
PMID: 33027220
PMCID: PMC8008742
NLM abbreviation: Pain
ISSN: 0304-3959
eISSN: 1872-6623
Publisher: United States
Grant note: IK2 RX002010 / RRD VA I01 RX002101 / RRD VA
Language: English
Date published: 04/01/2021
Academic Unit: Neurology; Molecular Physiology and Biophysics; Psychiatry; Stead Family Department of Pediatrics; Iowa Neuroscience Institute; Craniofacial Anomalies Research Center; Neurology (Pediatrics)
Record Identifier: 9984071799402771

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